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Dissecting Carotenoid-Related Protein Interaction Dynamics for Tailoring Healthier Crops

Final Report Summary - CAROTENACTORS (Dissecting Carotenoid-Related Protein Interaction Dynamics for Tailoring Healthier Crops)

Carotenoids represent a large and diverse class of biological compounds indispensable to photosynthetic organisms, since they have been exploited to maximize light harvesting and protect the photosynthetic machinery from photooxidative damage. Other organisms, like the vast majority of animals, do not produce carotenoids de novo, but incorporate them through their diet as a source of ornamental pigments and precursors of retinoids and vitamin A. Dietary consumption of carotenoids is associated with protection against a broad range of chronic human health conditions such as cancer, macular degeneration and cardiovascular disease. Carotenoids are also high value bioproducts of significant economic interest as natural colorants, nutraceuticals and food additives.

We now have a rather good picture of the core carotenoid biosynthetic pathway in plants, but much remains unknown about its regulation. The next grand challenge is therefore to increase our understanding of how carotenoid biosynthesis is regulated. Achieving this goal will lead to an expansion in our ability to breed healthier carotenoid-rich crops with enhanced photosynthesis and improved stress tolerance. CarotenActors addresses this challenge by studying carotenoid biosynthesis regulation in tomato (Solanum lycopersicum) fruit, a leading vegetable crop with a highly dynamic carotenoid metabolism.

The scientific objective of the CarotenActors project is to discover and validate regulatory mechanisms involved in the control of carotenoid biosynthesis. In this context, we performed a deep molecular and metabolic characterization of tomato fruits at different stages of maturation and ripening. We also generated stably transformed transgenic plants as subject models to test hypotheses. Among the main outcomes of the project, we discovered a novel regulatory mechanism that exploits core components of the inter-plant communication system that informs about vegetation proximity to regulate carotenoid biosynthesis during fruit ripening. Briefly, as tomato fruits ripe, they turn from green to red due to chlorophyll lost and carotenoid accumulation. Filtering of sunlight through the pericarp of green fruit causes a self-shading effect that prevents undue production of carotenoid pigments. Chlorophyll breakdown changes the quality of the filtered light and this promotes the degradation of phytochrome-interacting transcription factors (PIFs) that repress the gene encoding the main rate-determining enzyme of the fruit carotenoid pathway (phytoene synthase 1; PSY1), boosting carotenoid biosynthesis as self-shading attenuates. We also identified and characterized PIF1a, the fruit-specific transcription factor responsible for controlling PSY1 expression.

The knowledge gained during the CarotenActors project allowed us to rationally manipulate the regulation of the carotenoid pathway to obtain tomato fruits with higher amounts of total carotenoids. This demonstrates that the outcomes arising from CarotenActors could lead to increase the production of carotenoids in a number of other crops besides tomato.